Distinct inhibition of voltage-activated Ca2+ channels by delta-opioid agonists in dorsal root ganglion neurons devoid of functional T-type Ca2+ currents

Neuroscience. 2008 Jun 2;153(4):1256-67. doi: 10.1016/j.neuroscience.2008.03.031. Epub 2008 Mar 22.

Abstract

Both mu- and delta-opioid agonists selectively inhibit nociception but have little effect on other sensory modalities. Voltage-activated Ca(2+) channels in the primary sensory neurons are important for the regulation of nociceptive transmission. In this study, we determined the effect of delta-opioid agonists on voltage-activated Ca(2+) channel currents (I(Ca)) in small-diameter rat dorsal root ganglion (DRG) neurons that do and do not bind isolectin B(4) (IB(4)). The delta-opioid agonists [d-Pen(2),d-Pen(5)]-enkephalin (DPDPE) and deltorphin II produced a greater inhibition of high voltage-activated I(Ca) in IB(4)-negative than IB(4)-positive neurons. Furthermore, DPDPE produced a greater inhibition of N-, P/Q-, and L-type I(Ca) in IB(4)-negative than IB(4)-positive neurons. However, DPDPE had no significant effect on the R-type I(Ca) in either type of cells. We were surprised to find that DPDPE failed to inhibit either the T-type or high voltage-activated I(Ca) in all the DRG neurons with T-type I(Ca). Double immunofluorescence labeling showed that the majority of the delta-opioid receptor-immunoreactive DRG neurons had IB(4) labeling, while all DRG neurons immunoreactive to delta-opioid receptors exhibited Cav(3.2) immunoreactivity. Additionally, DPDPE significantly inhibited high voltage-activated I(Ca) in Tyrode's or N-methyl-d-glucamine solution but not in tetraethylammonium solution. This study provides new information that delta-opioid agonists have a distinct effect on voltage-activated Ca(2+) channels in different phenotypes of primary sensory neurons. High voltage-activated Ca(2+) channels are more sensitive to inhibition by delta-opioid agonists in IB(4)-negative than IB(4)-positive neurons, and this opioid effect is restricted to DRG neurons devoid of functional T-type Ca(2+) currents.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Analgesics, Opioid / pharmacology*
  • Animals
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, T-Type / physiology*
  • Dose-Response Relationship, Radiation
  • Drug Interactions
  • Electric Stimulation / methods
  • Enkephalin, D-Penicillamine (2,5)- / pharmacology*
  • Ganglia, Spinal / cytology*
  • Glycoproteins / metabolism
  • Lectins / metabolism
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / radiation effects
  • Naltrexone / analogs & derivatives
  • Naltrexone / pharmacology
  • Narcotic Antagonists / pharmacology
  • Neural Inhibition / drug effects*
  • Neurons, Afferent / drug effects*
  • Oligopeptides / pharmacology*
  • Patch-Clamp Techniques / methods
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Opioid, delta / metabolism
  • Versicans
  • omega-Conotoxin GVIA / pharmacology

Substances

  • Analgesics, Opioid
  • Cacna1h protein, rat
  • Calcium Channel Blockers
  • Calcium Channels, T-Type
  • Glycoproteins
  • Lectins
  • Narcotic Antagonists
  • Oligopeptides
  • Receptors, Opioid, delta
  • Vcan protein, rat
  • deltorphin II, Ala(2)-
  • Versicans
  • Naltrexone
  • Enkephalin, D-Penicillamine (2,5)-
  • omega-Conotoxin GVIA
  • naltrindole